A natural promoter variation of SlBBX31 confers enhanced cold tolerance during tomato domestication

Cold stress affects crop growth and productivity worldwide. Understanding the genetic basis of cold tolerance in germplasms is critical for crop improvement. Plants can coordinate environmental stimuli of light and temperature to regulate cold tolerance. However, it remains unknown which gene in germplasms could have such function. Here, we utilized genome-wide association study (GWAS) to investigate the cold tolerance of wild and cultivated tomato accessions and discovered that increased cold tolerance is accompanied with tomato domestication. We further identified a 27-bp InDel in the promoter of the CONSTANS-like transcription factor (TF) SlBBX31 is significantly linked with cold tolerance. Coincidentally, a key regulator of light signalling, SlHY5, can directly bind to the SlBBX31 promoter to activate SlBBX31 transcription while the 27-bp InDel can prevent S1HY5 from transactivating SlBBX31. Parallel to these findings, we observed that the loss of function of SlBBX31 results in impaired tomato cold tolerance. SlBBX31 can also modulate the cold-induced expression of several ERF TFs including CBF2 and DREBs. Therefore, our study has uncovered that SlBBX31 is possibly selected during tomato domestication for cold tolerance regulation, providing valuable insights for the development of hardy tomato varieties.

Automated summary

Cold stress globally affects crop growth and productivity. Understanding the genetic basis of cold tolerance in germplasms is crucial for crop improvement. This study utilized GWAS to investigate cold tolerance in tomato accessions and found that increased cold tolerance is associated with tomato domestication. The CONSTANS-like TF SlBBX31 with a 27-bp InDel in its promoter was identified as significantly linked with cold tolerance, and it was regulated by the light signaling regulator SlHY5. Loss of function of SlBBX31 impaired tomato cold tolerance. The study provides insights into the selection of SlBBX31 during tomato domestication and its potential for developing hardy tomato varieties.